Integrative Overview of the Herpetofauna from Serra Da Mocidade, a Granitic Mountain Range in Northern Brazil
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A peer-reviewed open-access journal ZooKeys 715: 103–159 (2017) Overview of herpetofauna from Serra da Mocidade 103 doi: 10.3897/zookeys.715.20288 CHECKLIST http://zookeys.pensoft.net Launched to accelerate biodiversity research Integrative overview of the herpetofauna from Serra da Mocidade, a granitic mountain range in northern Brazil Leandro J.C.L. Moraes1, Alexandre P. de Almeida2, Rafael de Fraga1, Rommel R. Rojas2, Renata M. Pirani1, Ariane A.A. Silva1, Vinícius T. de Carvalho2, Marcelo Gordo2, Fernanda P. Werneck1 1 Coordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo 2936, 69067-375, Manaus, Amazonas, Brazil 2 Departamento de Biologia, Universidade Federal do Amazonas, Av. General Rodrigo Octávio Jordão Ramos 3000, 69077-000, Manaus, Amazonas, Brazil Corresponding author: Leandro J.C.L. Moraes ([email protected]) Academic editor: A. Herrel | Received 14 August 2017 | Accepted 4 October 2017 | Published 22 November 2017 http://zoobank.org/FF11D309-E66F-43F5-95E3-148E1F0D5728 Citation: Moraes LJCL, Almeida AP, Fraga R, Rojas RR, Pirani RM, Silva AAA, de Carvalho VT, Gordo M, Werneck FP (2017) Integrative overview of the herpetofauna from Serra da Mocidade, a granitic mountain range in northern Brazil. ZooKeys 715: 103–159. https://doi.org/10.3897/zookeys.715.20288 Abstract The Brazilian mountain ranges from the Guiana Shield highlands are largely unexplored, with an under- studied herpetofauna. Here the amphibian and reptile species diversity of the remote Serra da Mocidade mountain range, located in extreme northern Brazil, is reported upon, and biogeographical affinities and taxonomic highlights are discussed. A 22-days expedition to this mountain range was undertaken during which specimens were sampled at four distinct altitudinal levels (600, 960, 1,060 and 1,365 m above sea level) using six complementary methods. Specimens were identified through an integrated approach that considered morphological, bioacoustical, and molecular analyses. Fifty-one species (23 amphibians and 28 reptiles) were found, a comparable richness to other mountain ranges in the region. The recorded as- semblage showed a mixed compositional influence from assemblages typical of other mountain ranges and lowland forest habitats in the region. Most of the taxa occupying the Serra da Mocidade mountain range are typical of the Guiana Shield or widely distributed in the Amazon. Extensions of known distribution ranges and candidate undescribed taxa are also recorded. This is the first herpetofaunal expedition that accessed the higher altitudinal levels of this mountain range, contributing to the basic knowledge of these groups in remote areas. Copyright Leandro J.C.L. Moraes et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 104 Leandro J.C.L. Moraes et al. / ZooKeys 715: 103–159 (2017) Keywords Amazonia, bioacoustics, biogeography, lowland forest, morphology, mountain, mtDNA, Pantepui, phy- logenetic relationships Introduction Scientific interest in mountain ranges arises primarily because they are characterized by a geographical isolation associated with differential availability of topographical, climatic, and edaphic conditions along the altitudinal gradients (Haslett 1997, Martinelli 2007, Körner et al. 2017). These characteristics provide ideal conditions for the development of unique evolutionary lineages and occurrence of a variety of endemic taxa (Lomolino 2001, Rull 2005, Hoorn et al. 2013, Nogué et al. 2013). This speciation hotspot pattern occurs in the mountain ranges of northern South America (Guiana Shield highlands), which lies on the ancient terrain of the Cratonic Guiana Shield (Hershkovitz 1969, Désamoré et al. 2014, Salerno et al. 2012, Bonaccorso and Guayasamin 2013). Despite a history of different concepts and geographic boundaries (Mayr and Phelps 1967, Huber 1988a, Kok 2013a), these high altitude areas are considered as a distinct biogeographic region (Morrone 2014), presenting biotic affinities with the megadiverse Amazon and Andean regions (Duellman 1979, Salerno et al. 2012, Mannion et al. 2014). Initial discoveries concerning the amphibian and reptile diversity from Guiana Shield highlands were reported by localized expeditions at the transition between the nineteenth and twentieth centuries (Boulenger 1900, Roze 1958a, b). Knowledge in- creased exponentially when helicopters facilitated access to remote mountains (Aubre- cht et al. 2012), leading to several expeditions focused on describing the assemblages of particular localities. Such studies brought to prominence several endemic taxa from the highlands (e.g., Gorzula 1992, Myers 1997, Myers and Donnelly 1992, 1996, 2001, 2008, MacCulloch et al. 2007, Barrio-Amorós and Brewer-Carias 2008, Kok 2008, 2009a, 2009b, 2010, 2013b, 2015, Kok and Rivas 2011, Kok et al. 2010, 2011, 2015), and some resulted in broad outlines of the main biogeographical patterns of these taxa (e.g., Hoogmoed 1979, Duellman 1999, Gorzula and Señaris 1999, McDi- armid and Donnelly 2005). More recently, studies have shown that diversification and evolutionary patterns of distinct species were associated with the landscape history of the region (Kok et al. 2012, 2017, Salerno et al. 2012, 2015, Vacher et al. 2017). While several intriguing patterns have been found for some highland lineages, such as recent diversification and low genetic divergence among mountains (Salerno et al. 2012, Kok et al. 2012, 2017), overall knowledge on the geographical and altitudinal distribution patterns of amphib- ians and reptiles from Guiana Shield highlands and their drivers are far from being fully understood. One of the main reasons is the occurrence of huge sampling gaps, mostly due to the short-term nature of inventories and to the difficult and costly access to highland areas, some of which remain unexplored (Aubrecht et al. 2012). The sampling deficiency in the Brazilian region of the Guiana Shield highlands highlights the impor- Overview of herpetofauna from Serra da Mocidade 105 tance of exploring these areas for biodiversity and biogeography assessments. Sampling in novel mountain ranges will most likely result in the discovery of new taxa and unique lineages, and geographical range extensions, all of which can contribute to the conserva- tion of these threatened regions (Rull et al. 2016). Furthermore, most specimens currently collected during biological inventories are identified using morphological characteristics. However, given the pervasive occur- rence of cryptic diversity (Vences et al. 2005, Vences and Wake 2007), particularly in Neotropical amphibians and reptiles (Fouquet et al. 2007a, c, Geurgas and Rodrigues 2010, Oliveira et al. 2016, Kok et al. 2016), other methods are being used to reveal the hidden diversity in remote areas with difficult access. For example, molecular tech- niques may contribute to indicate the presence of undescribed species and detect cryp- tic speciation through divergence in DNA sequences, and this short-term result might take longer to be achieved using a single taxonomic data source (Vences et al. 2005, Vences and Wake 2007, Fouquet et al. 2007a, Paz and Crawford 2012). Recently, a multidisciplinary initiative conducted an expedition (“Biodiversity of the Serra da Mocidade”) to inventory the biological diversity of distinct taxonomic groups in the poorly known region of the Serra da Mocidade, a remote granitic moun- tain range located in northern Brazil (INPA, 2016), highly isolated from other moun- tains and with difficult access. Here we present and discuss the diversity of amphib- ians and reptiles of the area and their biotic affinities, using an integrative approach combining morphological, bioacoustical and molecular analyses to identify specimens. We found remarkable records, and make observations concerning species taxonomy, ecology and distribution patterns in the Guiana Shield highlands region. Materials and methods Study area The Guiana Shield highlands region is located in northern South America, within the limits of Venezuela, Guyana, Suriname, and Brazil (Fig. 1), and is composed of moun- tain ranges covered by dense forests, shrubby vegetation or moss forests, surrounded by a lowland matrix of either tropical forests or savanna ecosystems (Mayr and Phelps 1967, Huber 1988b, McDiarmid and Donnelly 2005). These ancient mountains date to the Precambrian period (1.8–2.5 billion years) (Santos et al. 2003, Nogué et al. 2009, Kok 2013a), and have two main geological origins: sedimentary rocks, which are currently exposed as abrupt vertical elevations with tabular tops (called “tepuis”) and igneous-metamorphic rocks, which lie beneath the sedimentary rocks and may also be exposed as granitic uplifts with a mountain-like appearance (Steyermark 1986, Schubert and Briceño 1987, Huber 1995, Hoorn and Wesselingh 2010). This study was conducted at Serra da Mocidade (Figs 1, 2), a complex of gra- nitic mountains located in extreme northern Brazil, within the limits of Caracaraí municipality, Roraima state, with a mean altitudinal level of 1,000 m above sea level 106 Leandro J.C.L. Moraes et al. / ZooKeys 715: 103–159 (2017) Figure 1. Study area. Location of a the main Guiana Shield highlands region in northern South Amer- ica, and b the Serra da Mocidade mountain range. A larger scale map of mountain range c shows